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Official websites use. Share sensitive information only on official, secure websites. To test the hypothesis that drugs of abuse and their conditioned stimuli CSs enhance memory consolidation, the effects of post-training exposure to cocaine and nicotine were compared to the effects of post-training exposure to contextual stimuli that were paired with the effects of these drugs. Therefore, this study reports for the first time that contextual stimuli paired with cocaine and nicotine, like the drugs themselves, have the ability to enhance memory consolidation. This idea has been formalized by the hypothesis that reinforcers exert their behavioral effects by enhancing memory consolidation: a time-dependent process in which a memory trace becomes stabilized and less sensitive to interference White and Milner ; McGaugh and Roozendaal Biologically, this is significant because events that enhance memory consolidation also increase the probability that behaviors will be more likely to be repeated in the future White The experimental approach used to explore the memory enhancing function of reinforcers involves manipulations delivered immediately, or soon after, training on a given task White ; Rkieh et al. This is a key experimental requirement because it is believed that a memory trace is labile, and therefore sensitive to modulations, particularly during a critical period of minutes to hours that follow the experience of learning McGaugh Therefore, using this post-training approach, it has been demonstrated that reinforcers such as food Huston et al. An interesting question is whether cues paired with reinforcing stimuli via classical conditioning can also influence memory consolidation. These are usually referred to as conditioned stimuli CS , or conditioned reinforcers, depending on the behavioral effect of interest. For example, activation of drug-paired CSs enhance operant responses in the absence of drugs Di Ciano and Everitt , and can even maintain responding when delivered contingently Rescorla and Solomon ; Tunstall and Kearns Moreover, in place conditioning, when a drug reinforcer is administered in a specific context, the contextual CS gains the ability to attract the animal when in a drug-free state for review, see Tzschentke , and can induce ultrasonic vocalizations similarly to acute injections of the drug Ahrens et al. Drug-paired CSs also acquire the ability to elicit other behavioral responses e. While it has been repeatedly demonstrated that CSs established by conditioning with drugs of abuse can activate and maintain approach behavior, it is unclear whether these CSs can also modulate memory consolidation. Holahan and White found that post-training exposure to a fear provoking CS enhanced consolidation of a cue preference task. As well, Leong et al. This conclusion is further supported by evidence of enhanced acquisition of the Morris water maze by pretesting exposure to a morphine- or cocaine-paired context Zhai et al. The experiments presented in the current study were designed to test the hypothesis that drug CSs can enhance memory consolidation by comparing the effects of post-training drug administration to the effects of post-training exposure to contextual stimuli that were paired with the effects of the same drugs. Cocaine and nicotine were selected because they have been found previously to enhance memory consolidation Introini-Collison and McGaugh ; Beer et al. Contextual conditioning was selected because place preference studies performed in several laboratories, including ours, have consistently shown that a compartment paired with injections of cocaine will elicit an approach response in cocaine-free animals Bardo et al. Place preference studies with nicotine point to the same general conclusion Le Foll and Goldberg , , although the results with nicotine have been more variable Liu et al. The effects of post-training administration of cocaine and nicotine, and exposure to cocaine and nicotine CSs, were tested on a spontaneous object recognition OR task. This memory task is based on the natural tendency of rats to explore novel objects Ennaceur and Meliani ; Winters et al. Immediate post-sample cocaine enhanced OR memory Fig. The analysis of total object exploration was nonsignificant for the sample and choice phases data not shown. When cocaine injections were delayed by 6 h, there was no evidence of object memory, as the sample and choice phase discrimination ratios did not differ Fig. The denotes a significant difference when compared to the sample phase discrimination ratio. Experiment 5. Experiment 2. The denotes a significant difference compared to sample phase discrimination ratio. A final analysis ascertained whether the choice DR following post-training confinement in the cocaine-paired compartment was related to total locomotion displayed during the confinement period, and the correlation was not statistically significant. Immediate post-sample nicotine enhanced OR performance Fig. Multiple comparisons further indicated that rats only produced significantly higher discrimination ratios when injected with 0. The analysis of total object exploration was nonsignificant for the sample and choice phase data not shown. When nicotine 0. The denotes a significant difference compared to sample discrimination ratio. Multiple comparisons indicated that rats were significantly more active when injected with 0. Experiment 4. A final analysis ascertained whether choice DR following post-training confinement in the cocaine-paired compartment was related to total locomotion displayed during the confinement period, and the correlation was not statistically significant. During the test of conditioned place preference, rats significantly preferred the nicotine-paired chamber over the vehicle-paired chamber Fig. Multiple comparisons indicated that during habituation rats did not significantly prefer either chamber but spent significantly more time in the nicotine-paired chamber during the test of place preference. To test the hypothesis that incentive CSs enhance memory consolidation, this study compared the effects of post-training exposure to cocaine, nicotine, and contextual stimuli paired with the effects of these drugs on object memory in rats. Therefore, this study reports for the first time that contextual stimuli paired with drugs of abuse not only gain the ability to produce approach, but they also become capable of enhancing memory processes. Cocaine alters synaptic levels of dopamine, noradrenaline, and serotonin by blocking their transporters Carrera et al. Nicotine activates nicotinic acetylcholine receptors throughout the brain Deiana et al. Both drugs are abused Carrera et al. This prediction has been tested extensively in several species using various memory tasks Introini-Collison and McGaugh ; Sansone et al. As expected, both cocaine Fig. This strongly suggests that post-training administration of these drugs enhanced memory of the objects seen during the sample phase because of a selective action on consolidation rather than other memory processes such as encoding or retrieval Roozendaal and McGaugh Demonstrating that both post-sample cocaine and nicotine effectively enhanced OR memory was essential to test whether contextual stimuli paired with these drugs could also modify memory consolidation in the same task. During these pairings, the typical stimulation of motor activity was observed Figs. More important, using this within-subjects design, it was found that post-sample exposure to the cocaine Fig. Hence, other conditioning preparations are needed to explicitly explore the relationship between conditioned locomotion, conditioned approach, and conditioned memory modulation in the same animals Ettenberg ; Saunders et al. These results are essential to the interpretation of the data for three reasons. First, they rule out the possibility that OR was facilitated by some drug-induced nonspecific effects on perceptual, cognitive, or motor functions resulting from repeated administration during the conditioning period. Last, the findings exclude possible nonspecific effects linked to arousal or stress caused by confinement in the conditioning compartments. The parallel findings with cocaine and nicotine suggest that these drugs may modulate memory consolidation by activating overlapping neurochemical systems. One of these systems may be the basolateral amygdala Roozendaal et al. There is also evidence that the mesolimbic dopamine system may be involved. For example, the ventral tegmental area is a primary source of dopamine afferents to the basolateral amygdala, hippocampus, and prefrontal cortex Beninger ; Schultz et al. Central cholinergic systems could also play a role Vnek et al. The interesting possibility raised by the current results is that pathways of memory enhancement shared by acute cocaine and nicotine may also be involved in memory enhancement induced by exposure to their CS. In support of this hypothesis, there is evidence that the basolateral amygdala is required for the facilitation of memory consolidation induced by conditioned emotional stimuli Holahan and White , ; Goode et al. Mesolimbic dopamine may also play a role as it modulates conditioned responses to Pavlovian stimuli Parkinson et al. In conclusion, consistent with the memory consolidation hypothesis of drugs of abuse White , the present results suggest that contextual stimuli paired with the effects of cocaine and nicotine enhance memory consolidation. These data in rats identify a psychological function of cocaine- and nicotine-associated stimuli that is likely to impact the development and maintenance of addictive behaviors. A total of male Sprague—Dawley rats Charles River, Quebec, Canada , weighing between and g at the beginning of the experiments were individually housed in standard rat cages polycarbonate; All testing was conducted during the dark period. Rats had access to 25 g per day of standard rat chow, and water was available ad libitum in home cages. All experiments were approved by the Animal Care Committee of the University of Guelph and were performed in accordance with recommendations provided by the Canadian Council on Animal Care. Distinct visual marbled white and black pattern on the wall of one compartment and vertical white and black stripes on the wall of the other; objects external to the boxes including cabinets, tables, and computer and tactile one compartment in each chamber contained a black ceramic floor tile cues were maintained constant throughout the experiment. Black wire mesh covered the front of each compartment allowing for automatic video tracking EthoVision v3, Noldus, The Netherlands. The software was also used to create a virtual transition zone approximately the size of a g rat creating a third, middle compartment. Time spent in this virtual compartment was not included in data analysis. One arm was designated as the start arm and contained a guillotine door 18 cm from the rear of the arm to confine the rat at the start of a trial. The remaining two arms served as choice arms. The objects used were copies made from plastic, ceramic, and glass. Objects ranged in height from 10 to 20 cm and varied with respect to their visual and tactile qualities. Objects were fixed to the floor using odorless reusable adhesive putty. A JVC Everio digital camera was mounted on a tripod above the apparatus to record all trials. Experiment 1 was designed to assess the effect of acute post-sample cocaine administration on OR memory. Thirty-six rats were habituated to the empty Y-apparatus for 5 min on two consecutive days before the beginning of testing. The test trials began 24 h after the second habituation session. Each trial consisted of two phases: a sample phase and a choice phase, separated by a 72 h retention interval. Rats were always exposed to new, never-before-seen objects on each trial. During the sample phase, two identical novel objects were placed into the Y-apparatus at the end of each exploration arm. Each rat was placed in the start box, and the guillotine door was opened. Rats were allotted a maximum of sec to explore objects or were removed if 25 sec of total object exploration was achieved, whichever came first. All animals were tested at each dose of cocaine and the order of cocaine doses was counterbalanced using a Latin Square Design. Following the 72 h retention interval, rats experienced the choice phase, for which the Y-apparatus contained a copy of the original sample object in one arm and a novel object in the other. The choice phase lasted 2 min, and the time spent exploring the novel and familiar objects was recorded. Different object pairs were used for each trial, and the order of exposure to object pairs, as well as the designated sample and novel objects for each trial were counterbalanced. Conditioned locomotion was assessed on two separate tests. The second test occurred 72 h later and the same animals were tested in the alternate chamber. Of the 48 rats, 24 rats were tested on OR and 24 rats were only tested on conditioning. The rats tested on OR were habituated to the Y-apparatus on Days 9 and 10 of conditioning and were exposed to the sample phase prior to the first test of conditioned locomotion on Day The choice phase of OR occurred 72 h later Day The final test of OR occurred 72 h later Day Experiment 3 was designed to assess the effect of acute post-sample nicotine administration on OR memory. Experiment 4 was designed to assess the effect of post-sample exposure to a nicotine 0. A total of 48 rats were conditioned and tested on OR using the same procedures as in Experiment 2. Experiment 5 was designed to assess the effect of nicotine 0. Nicotine has been shown to produce both conditioned place aversion and preference at various doses; therefore, we designed this experiment to assess the reinforcing effects of 0. Twelve rats were habituated for 30 min to the conditioning chambers 24 h prior to the beginning of conditioning nicotine-paired chamber; vehicle-paired chamber. At the beginning of conditioning, rats received either vehicle or 0. The chambers of the apparatus were counterbalanced across rats. All animals received a total of five conditioning sessions with vehicle and 5 with 0. Place preference was assessed 24 h following the final conditioning day. All drugs were injected intraperitoneally i. Vehicle sterile 0. The doses of these two drugs were selected because of their known stimulatory properties Zavala et al. Comparison between the sample and choice phase discrimination ratios was used as an index of successful memory for objects. For all OR experiments, total object exploration was also analyzed for both the sample and choice phases as a control measure of general exploratory behavior. The values of nonsignificant analyses are not reported. One rat from Experiment 1 and one from Experiment 3 had to be removed from data analysis because of complete inactivity during OR testing. One rat from Experiment 5 had to be removed because its habituation activity was two SDs above the mean. As a library, NLM provides access to scientific literature. Learn Mem. Find articles by Michael Wolter. Find articles by Ethan Huff. Find articles by Talia Speigel. Find articles by Boyer D Winters. Find articles by Francesco Leri. Received Oct 3; Accepted Dec Open in a new tab. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel.
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